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Gibberellin-induced DELLA recognition by the gibberellin receptor GID1

Nature volume 456, pages 459–463 (2008)Cite this article

Abstract

Gibberellins control a range of growth and developmental processes in higher plants and have been widely used in the agricultural industry. By binding to a nuclear receptor, GIBBERELLIN INSENSITIVE DWARF1 (GID1), gibberellins regulate gene expression by promoting degradation of the transcriptional regulator DELLA proteins, including GIBBERELLIN INSENSITIVE (GAI). The precise manner in which GID1 discriminates and becomes activated by bioactive gibberellins for specific binding to DELLA proteins remains unclear. Here we present the crystal structure of a ternary complex of Arabidopsis thaliana GID1A, a bioactive gibberellin and the amino-terminal DELLA domain of GAI. In this complex, GID1A occludes gibberellin in a deep binding pocket covered by its N-terminal helical switch region, which in turn interacts with the DELLA domain containing DELLA, VHYNP and LExLE motifs. Our results establish a structural model of a plant hormone receptor that is distinct from the mechanism of the hormone perception and effector recognition of the known auxin receptors.

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Figure 1: Structure of the GA 3 –GID1A–DELLA complex.
Figure 2: Architecture of GID1A.
Figure 3: Recognition of GA 3 by GID1A.
Figure 4: Architecture of the DELLA domain of GAI.
Figure 5: Recognition of the DELLA domain by GID1A.
Figure 6: A model of GA-regulated GID1–DELLA protein interactions.

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Accession codes

Primary accessions

Protein Data Bank

Data deposits

Structure coordinates and structural factors are deposited in the Protein Data Bank under accession numbers 2ZSH (GA3–GID1A–DELLA) and 2ZSI (GA4–GID1A–DELLA).

References

  1. Yabuta, T. & Sumiki, Y. On the crystal of gibberellin, a substance to promote plant growth. J. Agric. Chem. Soc. Japan 14, 1526 (1938)

    Google Scholar 

  2. Radley, M. Occurrence of substances similar to gibberellic acid in higher plants. Nature 178, 1070–1071 (1956)

    Article  ADS  CAS  Google Scholar 

  3. Yamaguchi, S. Gibberellin metabolism and its regulation. Annu. Rev. Plant Biol. 59, 225–251 (2008)

    Article  CAS  Google Scholar 

  4. MacMillan, J. Occurrence of gibberellins in vascular plants, fungi, and bacteria. J. Plant Growth Regul. 20, 387–442 (2002)

    Article  Google Scholar 

  5. Ueguchi-Tanaka, M. et al. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437, 693–698 (2005)

    Article  ADS  CAS  Google Scholar 

  6. Nakajima, M. et al. Identification and characterization of Arabidopsis gibberellin receptors. Plant J. 46, 880–889 (2006)

    Article  CAS  Google Scholar 

  7. Peng, J. et al. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 11, 3194–3205 (1997)

    Article  CAS  Google Scholar 

  8. Silverstone, A. L., Ciampaglio, C. N. & Sun, T.-p. The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10, 155–169 (1998)

    Article  CAS  Google Scholar 

  9. McGinnis, K. M. et al. The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15, 1120–1130 (2003)

    Article  CAS  Google Scholar 

  10. Sasaki, A. et al. Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299, 1896–1898 (2003)

    Article  ADS  CAS  Google Scholar 

  11. Dill, A., Jung, H.-S. & Sun, T.-p. The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc. Natl Acad. Sci. USA 98, 14162–14167 (2001)

    Article  ADS  CAS  Google Scholar 

  12. Itoh, H., Ueguchi-Tanaka, M., Sato, Y., Ashikari, M. & Matsuoka, M. The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14, 57–70 (2002)

    Article  CAS  Google Scholar 

  13. Griffiths, J. et al. Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis . Plant Cell 18, 3399–3414 (2006)

    Article  CAS  Google Scholar 

  14. Willige, B. C. et al. The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis . Plant Cell 19, 1209–1220 (2007)

    Article  CAS  Google Scholar 

  15. Ueguchi-Tanaka, M. et al. Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19, 2140–2155 (2007)

    Article  CAS  Google Scholar 

  16. Pysh, L. D., Wysocka-Diller, J. W., Camilleri, C., Bouchez, D. & Benfey, P. N. The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J. 18, 111–119 (1999)

    Article  CAS  Google Scholar 

  17. Silverstone, A. L. et al. Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis . Plant Cell 13, 1555–1565 (2001)

    Article  CAS  Google Scholar 

  18. Dill, A., Thomas, S. G., Hu, J., Steber, C. M. & Sun, T.-p. The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16, 1392–1405 (2004)

    Article  CAS  Google Scholar 

  19. Fu, X. et al. The Arabidopsis mutant sleepy1gar2–1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16, 1406–1418 (2004)

    Article  CAS  Google Scholar 

  20. Zentella, R. et al. Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis . Plant Cell 19, 3037–3057 (2007)

    Article  CAS  Google Scholar 

  21. Iuchi, S. et al. Multiple loss-of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. Plant J. 50, 958–966 (2007)

    Article  CAS  Google Scholar 

  22. Talon, M., Koornneef, M. & Zeevaart, J. A. D. Endogenous gibberellins in Arabidopsis thaliana and possible steps blocked in the biosynthetic pathways of the semidwarf ga4 and ga5 mutants. Proc. Natl Acad. Sci. USA 87, 7983–7987 (1990)

    Article  ADS  CAS  Google Scholar 

  23. Derkx, M. P. M., Vermeer, E. & Karssen, C. M. Gibberellins in seeds of Arabidopsis thaliana: biological activities, identification and effects of light and chilling on endogenous levels. Plant Growth Regul. 15, 223–234 (1994)

    Article  CAS  Google Scholar 

  24. King, K. E., Moritz, T. & Harberd, N. P. Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159, 767–776 (2001)

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Dill, A. & Sun, T.-p. Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana . Genetics 159, 777–785 (2001)

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Lee, S. et al. Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following inhibition. Genes Dev. 16, 646–658 (2002)

    Article  CAS  Google Scholar 

  27. Cheng, H. et al. Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131, 1055–1064 (2004)

    Article  CAS  Google Scholar 

  28. Tyler, L. et al. DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis . Plant Physiol. 135, 1008–1019 (2004)

    Article  CAS  Google Scholar 

  29. Ileperuma, N. R. et al. High-resolution crystal structure of plant carboxylesterase AeCXE1, from Actinidia eriantha, and its complex with a high-affinity inhibitor paraoxon. Biochemistry 46, 1851–1859 (2007)

    Article  CAS  Google Scholar 

  30. Thomas, S. G., Phillips, A. L. & Hedden, P. Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc. Natl Acad. Sci. USA 96, 4698–4703 (1999)

    Article  ADS  CAS  Google Scholar 

  31. Varbanova, M. et al. Methylation of gibberellins by Arabidopsis GAMT1 and GAMT2. Plant Cell 19, 32–45 (2007)

    Article  CAS  Google Scholar 

  32. Crick, F. H. C. The packing of α-helices: simple coiled coils. Acta Crystallogr. 6, 689–697 (1953)

    Article  CAS  Google Scholar 

  33. Hakoshima, T. in Nature Encyclopedia of the Human Genome Vol. 3, 679–683 (Nature Publishing Group, 2003)

    Google Scholar 

  34. McSteen, P. & Zhao, Y. Plant hormones and signaling: common themes and new developments. Dev. Cell 14, 467–473 (2008)

    Article  CAS  Google Scholar 

  35. Ho, M. S., Ou, C., Chan, Y.-r., Chien, C.-T. & Pi, H. The utility F-box for protein destruction. Cell. Mol. Life Sci. 65, 1977–2000 (2008)

    Article  CAS  Google Scholar 

  36. Dharmasiri, N., Dharmasiri, S. & Estelle, M. The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445 (2005)

    Article  ADS  CAS  Google Scholar 

  37. Kepinski, S. & Leyser, O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451 (2005)

    Article  ADS  CAS  Google Scholar 

  38. Thines, B. et al. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661–665 (2007)

    Article  ADS  CAS  Google Scholar 

  39. Chini, A. et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666–671 (2007)

    Article  ADS  CAS  Google Scholar 

  40. Tan, X. et al. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640–645 (2007)

    Article  ADS  CAS  Google Scholar 

  41. Alberts, B. et al. in Molecular Biology of the Cell 5th edn, 395–396 (Garland Science, 2008)

    Google Scholar 

  42. LeMaster, D. M. & Richards, F. M. 1H–15N heteronuclear NMR studies of Escherichia coli thioredoxin in samples isotopically labeled by residue type. Biochemistry 24, 7263–7268 (1985)

    Article  CAS  Google Scholar 

  43. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307–326 (1997)

    Article  CAS  Google Scholar 

  44. Weeks, C. M. et al. Towards automated protein structure determination: BnP, the SnB-PHASES interface. Z. Kristallogr. 217, 686–693 (2002)

    CAS  Google Scholar 

  45. Terwilliger, T. SOLVE and RESOLVE: Automated structure solution, density modification and model building. J. Synchrotron Radiat. 11, 49–52 (2004)

    Article  CAS  Google Scholar 

  46. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004)

    Article  Google Scholar 

  47. Brünger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905–921 (1998)

    Article  Google Scholar 

  48. Davis, I. W. et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375–W383 (2007)

    Article  ADS  Google Scholar 

  49. Weiner, M. P. et al. Site-directed mutagenesis of double-strand DNA by the polymerase chain reaction. Gene 151, 119–123 (1994)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank S. Terawaki and T. Mori for technical advice and J. Tsukamoto for technical support in performing the matrix-assisted laser desorption/ionization time-of-flight mass spectroscopy analysis, and the beamline staff of BL41XU of SPring-8 at Harima for help with the data collection. We also acknowledge A. Isogai for advice and encouragement. This work was supported by a research grant in the natural sciences from the Mitsubishi Foundation, Japan (to T.H.), and in part by a Grant-in-Aid for Scientific Research (A) and Scientific Research on Priority Areas from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan (to T.H.). This work was also supported in part by grants from the National Science Foundation of the United States (IBN-0348814 to T.-p.S.). K.M. is a recipient of a postdoctoral fellowship for Young Scientists from the Japan Society for the Promotion of Science and an international research fellowship from the Global COE Program in NAIST (Frontier Biosciences: strategies for survival and adaptation in a changing global environment) from MEXT of Japan.

Author Contributions K.M., T.-p.S. and T.H. conceived and designed the project. T.-p.S. provided all cDNA and constructs as well as expertise in the GA signalling mechanism. Y.H., K.M. and T.H. were responsible for construct design for protein preparation. K.M. was responsible for subcloning and execution of protein biochemistry, crystallization and data collection, helped by Y.H. and directed by T.H. Y.H. solved and refined the complex structures. K.M. performed binding studies with GID1A and DELLA variants, as well as circular dichroism measurements, directed by Y.H. Y.H, K.M. and T.H. interpreted data and T.H. wrote the manuscript.

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  1. Kohji Murase and Yoshinori Hirano: These authors contributed equally to this work.

Authors and Affiliations

  1. Structural Biology Laboratory, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0192, Japan ,

    Kohji Murase, Yoshinori Hirano & Toshio Hakoshima

  2. Department of Biology, Duke University, Durham, North Carolina 27708, USA,

    Kohji Murase & Tai-ping Sun

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Correspondence to Toshio Hakoshima.

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Murase, K., Hirano, Y., Sun, Tp. et al. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456, 459–463 (2008). https://doi.org/10.1038/nature07519

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